Redescription of Halgerda graphica Basedow and Hedley, 1905, with Observations on External Morphological Variation within Selected Species of Halgerda (Mollusca: Nudibranchia)

14 Pages·2003·7.8 MB·English

by  Shireen J Fahey

PROCEEDINGS OFTHE CALIFORNIAACADEMY OF SCIENCES
Volume 54. No. 23. pp. 393-406. 12 figs. November 14, 2003
Redescription of Halgerda graphica Basedow and Hedley, 1905,
with Observations on External Morphological Variation within
Selected Species ofHalgerda (MoUusca: Nudibranchia)
Shireen J. Fahey and Terrence M. Gosliner
DepartmentofInvertebrateZoologyandGeology
CaliforniaAcademy ofSciences
Golden GatePark, San Francisco, California 94118, USA
Halgerda graphica Basedow and Hedley, 1905 is redescribed based on examination
of two specimens; one collected in 1904 from Middle Harbour, Sydney, Australia,
housed attheAustralian Museum, Sydney, and anotherspecimen collected in 1990,
fromPort Moorowie, nearthetypelocality (KangarooIsland,SouthAustralia).The
reproductive system is described and illustrated for the first time. This species has
frequently been misidentified due to having similar external morphology to other
Halgerda species. A comparison is made to those species. Halgerda graphica has a
unique combination ofexternal and internal characters that confirm itas a distinct
Halgerdaspecies.Theexternalcharactersincludea"hieroglyphic"patternofyellow
and black markings on the notum, small, similar-size dark spotson the ventralsur-
face, a small, sparse, dark-colored gill and rhinophores with a white base, dark tip
and a dark line on the posterior side. The external color variations of Halgerda
dichromis Fahey and Gosliner, 1999,H. Okinawa Carlson and Hoff, 2000andH. wil-
leyi Eliot, 1904 are also described, illustrated and compared to externally similar
species. It is the unique combination ofexternal morphological characters such as
the color and pattern on the notum, the structure and color of the gills and
rhinophores that help to distinguish each species, although examination ofinternal
morphology can confirm the identification.
Basedow andHedley (1905) describedthenudibranchHalgerdagraphicafromtwo specimens
dredged offAntechamber Bay, Kangaroo Island, SouthAustralia. They had at the time examined a
third specimen, which, although not included in the original description, they indicated that it
belonged to theirnew species. The original description ofthe external andradularmorphologies of
the specimens were quite detailed, but the authors did notprovide adescription ofthereproductive
morphology. This species did not show up again until 1990. In the meantime, other authors (e.g.,
Coleman 1975, 2001; Kay 1979; Kay and Young 1969; Wells and Bryce 1993) have erroneously
attributed the name Halgerda graphica to other species.
The present study describes two additional specimens ofHalgerda graphica; the single spec-
imen mentioned by Basedow and Hedley, collected in approximately 1904 at Middle Harbour,
.Sydney, and an additional specimen collected by N. Holmes in 1990 from Port Moorowie, Yorke
Peninsula, SouthAustralia.
The nudibranch genus Halgerda Bergh, 1880 has been studied extensively in recent years
(Rudman 1978; Willan and Brodie 1989; Carlson and Hoff 1993, 2000; GosUnerand Fahey 1998;
' Contactauthor: [email protected]
393
394 PROCEEDINGS OFTHE CALIFORNIAACADEMY OF SCIENCES
Volume 54, No. 23
Fahey and Gosliner 1999a, 1999b, 2000, 2001a, 2001b). Since 1998, the number of described
species increased from 14 to 35. Among Halgerda species are several that display external color
variation in specimens from similar habitats and from varying geographic ranges. Four species, in
particular, seem to be most commonly confused: Halgerda graphica, H. willeyi, H. Okinawa
Carlson and Hoff, 2000, andH. dichromis Fahey and Gosliner, 1999. The present study illustrates
the color variations that can cause misidentification of these four species in the field and then
makes comparisons with the externally most similarspecies. Field notes andphotographic records
ofmany observers, both amateur and professional, provide the basis ofthe discussion on external
color variation presented in this paper.
Descriptions of taxa
Labiostomata Valdes, 2002
Family Discodorididae Bergh, 1891
Genus Halgerda Basedow and Hedley, 1905
(Type species: Halgerdafonnosa Bergh, 1880, by monotypy)
Halgerdagraphica Basedow and Hedley, 1905
(Figs 1-3)
—
TypeMaterial. Thetype material isprobably lost; it is notattheAustralianMuseum. The
type locality is Kangaroo Island, South Australia. The authors (Basedow and Hedley 1905) men-
tion an additional specimen deposited at the Australian Museum, Sydney (CI8168, Location
#016276, collector not named) from Middle Harbour near Sydney, in September 1904. This spec-
imen was examined and is both de—scribed below and hereby designated as the neotype.
Other materialexamined. SouthAustralian Museum, TD16542, one specimen, dissect-
ed, Port Moorowie, Yorke Peninsula, South Australia. 10 m deep, collected by Nigel Holmes, 15
December 1990.
—
Externalmorphology. Becausethere are nophotographs ordrawings available forspec-
imen C18168 (1904), the following is a description of the specimen collected in 1990 by N.
Holmes. This specimen is nearly identical to the drawing and description of Halgerda graphica
provided by Basedow and Hedley in 1905 (Fig. lA).
The preserved animal is 28 mm in length. The body profile is rounded, convex (Fig. IB) and
the dorsum has a low-ridged pattern. There are no small marginal tubercles. There is a low central
ridge running the length of the dorsum that splits into several smaller ridges as it nears the gill
pocket. The ridges have orange-yellow crests. The background color ofthe dorsum is gray-white.
Between the ridges are black spots with some spots circled or semi-circled with the same yellow
coloras the ridges. The dark spots closestto the mantle edge are smallerthanthose on the dorsum.
The mantle margin is translucent white when vieweddorsally, but when viewed ventrally, ayellow
margin is apparent. On the underside ofthe mande and along the side ofthe foot are dark spots of
various sizes. The foot margin is yellow (Fig. IC). The oral tentacles are long and tapered.
The long rhinophores have a bulging club that is tapered at the tips. The club is angled poste-
riorly and there is darkbrowntoblackcoloration aroundthe top halfofthe club up to the tip. The
base is translucent white and there is a dark line on the posterior side of the rhinophores that
extends from the base to the tip.
The bipinnate gill lies flat over the dorsum and is moderately pinnate. Each ofthe four main
gill rachae has a brown stripe on the anterior sides. The anal papilla is long and is the same color
as the body.
FAHEYAND GOSLINER: HALGERDA GRAPHICA 395
Figure 1.A.HalgerclagraphicaBasedowandHedley,
Vcl XXIX PUte Ifl S1o9u05t,hfAursotmratlhieanoriMguisnaelumco,lo(rTpDla1t6e5.4B2.),Hpahlogteorgdraagprhaepdhaincad
collected by N. Holmes, 1990. Dorsal view. C. Ventral
—
Buccalarmature. The buccal mass
has dark spots. The labial cuticle is smooth
and devoid of any jaw rodlets. The radular
sac is elongate and extends well behind the
posteriorend ofthe buccal mass. The radular
formulaofthe specimencollectedin 1990is:
43x30.0.30 (TD16542) (Fig. 2A). The radu-
larformulaofthe specimencollectedin 1904
could not be determined due to poor preser-
vation and deterioration of the radula. The
three outer teeth are much smaller than the
inner and middle lateral teeth and the outer
twoteeth havetiny denticles (Fig. 2B). The 8
or so inner lateral teeth are smaller and have
shorter hooks than the middle lateral teeth
(Fig. 2C) and are arranged in a shallow V-
shaped pattern in the center of the radula.
Themiddlelateralteetharehamate (Fig. 2D)
4«i tf;ni.i«%u with long, pointed hooks. They have a flat-
HALGERDA GRAPHICA. Bajcdou A Hcdicy. tened flange, which overlaps the adjacent
tooth. —
Reproductive System. The repro-
ductive system is triaulic (Fig. 3). The long
ampulla is tubular, curved into a complete
loop and protrudes away from the bursa and
prostate. The ampulla narrows into the post-
ampullary duct, whichbifurcates intothe vas
deferens and oviduct. The long oviduct
enters the female gland mass. The female
gland mass is about the same size as the
bursa copulatrix. The long vas deferens sep-
arates from the ampulla and widens into the
glandular prostate. The prostate consists of
ct
/ fc- twodistinctglandulartypes andtheyarewell
1? differentiated as in most other members of
Halgerda. Themuscularportion ofthe defer-
ent duct leaves the distal prostate in a long
duct that curves into one loop and multiple
half-loops, then enters the wide penial bulb.
The long uterine duct emerges from the
female glandmass andjoins the ovoidrecep-
taculum seminis near its base. The duct con-
396 PROCEEDINGS OFTHE CALIFORNIAACADEMY OF SCIENCES
Volume 54, No. 23
Figure2.RadularmorphologyofHolgerdagraphica(TD16542).A.Entireradula.Scale=2|im.B.Outerlaicialiccih.
Scale=50pm. C. Innerlateralteeth. Scale= 100|am. D. Middle lateral teeth. Scale=20|im.
necting the receptaculum and the bursa is long and coiled. The receptaculum seminis is much
smallerthan the thin-walled spherical bursacopulatrix. It lies underthe bursa, but is notembedded
in the prostate. The prostate does not completely coverthe bursacopulatrix as is common in other,
more highly derived species ofHalgerda, but lies in a thin layerover two-thirds ofthe bursa. The
vaginal duct that emerges from the base ofthe bursa copulatrix is long and thin. Near its exit into
the bulbous vagina that is adjacent to the base of the penial sheath, is a muscular sphincter. The
vaginahas long folds in the walls and tubercularglands on the exterior. The common genital aper-
ture is wide, large and has long fleshy folds that extendthrough the body wall. The opening ofthe
female gland mass is adjacent to the genital aperture.
FAHEYAND GOSLINER: HALGERDA GRAPHICA 397
Discussion
Although Basedow and Hedley (1905)
described the external and radular morphology
of Halgerda graphica, these authors did not
illustrate ordescribe the reproductive morphol-
ogy. Despitethis,basedontheuniquecolorpat-
tern ofthis species, there is litde doubt that the
specimens examined for this study are
Halgerda graphica. Other authors (Coleman
1975, 2001; Kay 1979; Kay and Young 1969;
Wells and Bryce 1993) have erroneously attrib-
uted the name Halgerda graphica to other
species. Wells and Bryce, mislabeled a speci-
men of Halgerda gunnessi as H. graphica
Basedow and Hedley, 1905; Kay misidentified
a specimen ofH. terramtuentis as H. graphica;
Figure3.ReproductivemorphologyoiHalgerdagrapli- and Coleman (1975, 2001) misidentified a
ica.Abbreviations: am=ampulla,be=bursacopulatrix, dd specimen ofH. willeyi as H. graphica.
=deferentduct, fgm=femaleglandmass,ga=genital atri-
um,p=penis,rs=receptaculumseminis. v=vagina. Scale Examination ofthe reproductive morphol-
=0.25mm. ogy reveals similar characters to other
Halgerda such as a two-part prostate, a long,
convoluted deferentduct, abulbous penial sheath and a wide, muscularvagina. Radularcharacters
also have similarities to other Halgerda species. Those characters are hooked mid-lateral teeth,
finely denticulate outerteeth that are much smallerthan the remaining teeth, and small inner later-
al teeth.
Because of the similarity in external coloration of Halgerda graphica to H. gunnessi Fahey
andGosliner, 2001, H.johnsonorum Carlson andHoff, 2000andH. willeyiEliot, 1904, these three
are herein compared and contrasted to H. graphica. However, because Carlson and Hoff (2000)
have already comparedH. graphicatoH. Okinawa, we will notrepeatwhatthey havealreadydone.
Neitherwill we repeat what Fahey and Gosliner said when they compared H. gunnessi to H.john-
sonorum and to H.fonnosa Bergh, 1880, nor what Carlson and Hoff(2000) had to say when they
comparedH.johnsonorum toH. willeyi. Rather, we encourage reference totheirrespective papers.
Here we concentrate on comparingthe external morphology ofHalgerdagraphica to its most sim-
ilar species.
All four species ofgreatest concern to us, Hcdgerda graphica, H. gunnessi, H. johnsonorum
andH. willeyi, have awhite orgray-white groundcolorwith yellowto yellow-orange ridge crests.
Halgerda graphica has low ridges without tubercles as do H. gunnessi and H.johnsonorum. Only
H. willeyi has prominent tubercles. Although both H. graphica and H. johnsonorum have dark
spots or markings in the ridge concavities, only H. graphica has the "hieroglyphic markings"
described by Basedow and Hedley. These markings consist ofa dark spot at the center ofthe con-
cavity surrounded by darkcircles andlines (Fig. 1). The othertwo species, H. gunnessiandH. wil-
leyi may also have dark lines ormarkings, but both lack the associated spots.
The coloration of the mantle edge also distinguishes these four species. Halgerda graphica
does not have perpendicular dark markings along the mantle edge, but the edge markings of H.
johnsonorum appear as continuous lines, which extend upward and into the ridge concavities on
thedorsum. Thedarkperpendicularlines on themantle margin ofH. willeyialsoextendup intothe
398 PROCEEDINGS OFTHE CALIFORNIAACADEMY OF SCIENCES
Volume 54, No. 23
ridge cavities, but they are more numerous when compared to H. graphica. Halgerda gunnessi
does not have marginal lines (see Fahey and Gosliner 2001).
The ventral surfaces ofthe four species are not similar in that there are irregularly scattered
dark spots without lines only on Halgerda graphica. Halgerdajohnsouorum and Halgerda willeyi
have black lines; H. gunnessi has no markings on its ventrum.
The coloration on the rhinophores andgills differs among the species. Halgerda graphica has
dark coloration on the tips ofthe rhinophores and a dark line on the posterior side. This is similar
toH. gunnessi. The other species have eitherdark spots (H.johnsonoruni, H. willeyi) ordark spots
plus a dark stripe on the rhinophores (H.johnsonoruni) and large gills. The gill ofH. graphica is
small and darkly colored. The gill ofH. willeyi is sparsely pinnate with dark speckles. The gill of
H.johnsonoruni is large and has dark spots, and the gill ofH. gunnessi is large, feathery and has
dark lined branches and a dark tip.
With regard to the internal moiphology. Halgerda graphica has radular characters similar to
those ofH. gunnessi and H. willeyi. All three also have three small outer teeth. H.johnsonoruni is
distinct, having six outer teeth, with the penultimate being bifid. Halgerda graphica has two fine-
ly denticulate outer lateral teeth; the outer three ofH. willeyi and H. gunnessi are not denticulate.
The reproductive morphology ofHalgerdagraphica is most similartoH. willeyi. The obvious
differences betweenthe two arethatthedeferentductofH. graphicais muchlongerand morecon-
volutedthan inH. willeyiandthe vaginal ductofH. graphica is muchwiderwith the vagina, being
much larger with tubercular glands on the exterior. A glandular vagina is not found in any ofthe
other three species. Both Halgerda graphica and H. gunnessi have a vaginal sphincter.
The present study confirms the combination ofexternal and internal morphological characters
that identify Halgerda graphica and distinguish it from the four externally most similar species.
The external characters thatdistinguish this species in the field are: the "hieroglyphic" yellow and
black markings on the dorsum, no dark lines on the mantle edge, dark-tipped rhinophores with a
posterior medial line, a small, dark gill and small, dark spots on the ventral surface.
Halgerda dichromis Fahey and Gosliner, 1999
(Figs. 4-5)
—
Material examined. V8234, one specimen, dissected, 42 mm, Scottburgh, Kwazulu,
m
Natal, SouthAfrica, 25 deep, collectedbyV. Eraser, 15 January 2000;V8233, one specimen, dis-
sected, 20 mm. Park Rynie, KwaZulu, Natal, South Africa, 25 m deep, collected by V. Eraser, 28
December 1999; V8232. one specimen, dissected. 16 mm. Park Rynie. KwaZulu, Natal, South
m
Africa, 25 deep, collected by—V. Eraser. 21 January 2000.
External morphology. The external morphology of the specimens examined for this
study are as describedby Fahey and Goslinerwith some colorvariation. The variation includes the
presence of dark half-lines or spots on the dorsum of some specimens, in place of a heavy, dark
line. The morejuvenile specimens may not have any dark markings at all. Variations in the exter-
nal color within this species ar—e shown in Figures 4A-C.
Radular morphology. There were no differences noted in the radular morphology
between the recent specimens examined (Figs 5A-D) and Fahey and Gosliner's (1999) original
description and line drawings.—Figure 5A-D are the first SEMs ofthe radula ofthis species.
ReproductiveSystem. There werenodifferencesinthe sexually mature specimensexam-
ined for this study (Fig. 6) and Fahey and Gosliner's (1999) original description of Halgerda
dichromis.
—
Remarks. Halgerda dichromis was described from a single specimen collected in 1980
FAHEYAND GOSLINER: HALGERDA GRAPHICA 399
Figure4.ColorvariationofHalgenladichwinis.A-C.Photographedandcollectedby
V.Fraser,2000.
from Durban Harbor, SouthAfrica. Since the original description, additional specimens have been
collected and/or photographed from the same locality (present study) and, thus, allow a further
examination ofthe species.
Halgerda dichromis has a variable external coloration (Figs. 4A-C). The coloration of the
holotype includes orange and black lines that form a reticulate pattern on the notum (Fahey and
Gosliner 1999). Other patterns include having only orange or yellow lines with dark lines or
splotches and without dark markings at all, particularly on morejuvenile specimens.
Halgerdadichromis externally is mostsimilartoH.formosa (see Fahey and Gosliner 1999 for
details).
Halgerda Okinawa Carlson and Hoff, 2000
(Figs. 6-8j
—
Material Examined. CASIZ 144092, one specimen, 80 mm, dissected. Izu Peninsula,
Japan. 22m depth, collectedbyR. Nakano,April2000; CASIZ 144093, one specimen,46mm, dis-
sected. Izu Peninsula, Japan. 20 m depth, collected by R. Nakano, May 2000; CASIZ 144097, one
specimen, 50mm, dissected. Iz—uPeninsula,Japan. 22 mdepth, collectedby R. Nakano,April2000.
External morphology. The external morphology of the specimens examined from the
Izu Peninsula have the same range ofvariation as noted in the original description ofH. Okinawa
(Carlson and Hoff, 2000). Those variations include number, length and width ofthe dark streaks,
numberoflines on the innersurfaceofthebranchiaand presenceofayellow mantlemarginonthe
specimens examined forthis study. One ofthe specimens we examined from the Izu Peninsulahas
apalershadeofwhiteon thedorsum withpaleyellowtubercles (Fig. 7A).Theotherspecimen(Fig.
400 PROCEEDINGS OF THE CALIFORNIAACADEMY OF SCIENCES
Volume 54, No. 23
Figure5. Radularnioiphnlotiy o(Halgerdadichromis(V8233).A. Innerlateral teeth. Scale= 10|im. B. Middlelateral
teeth. Scale=50.8|am. C. Middle lateral teeth. Scale=50.8|am. D. Outerlateral teeth. Scale= 10|am.
7B) matched the original description from
Okinawa.AspecimenfromLembeh Strait(Fig.
7C) had few dark Hnes but more spots that the
more commonly found specim—en (Figs 7D-E).
Radularmorphology. There were no
differences noted in the radular morphology
between the recent specimens examined (Fig.
8) and Carlson and Hoff's (2000) original
description. —
Reproductive morphology. The
reproductive morphology of the specimens
examined for the present study (Fig. 9) were
nearly identical tothe original description The
.
Figure 6. Reproductive morphology of Halgerda exception is that the vagina is wider in the
dichromis (V8234). Abbreviations: am = ampulla, be = specimens we examined than was illustrated
bursa copulatrix, dd = deferent duct, fgm = female gland and drawn by C—arlson and Hoff(2000).
mass,ga=genitalatrium,p=penis,rs=receptaculumsem- Renlvrks. Since the original descrip-
inis,V=vagina. Scale=0.8mm.
tion of H. Okinawa, additional specimens col-
lected from the Izu Peninsula, Japan and pho-
FAHEYAND GOSLINER: HALGERDA GRAPHICA 401
?3I
^^^^^^^H^
'^^N^^K'"^i^l
asi-i^^!!^^^" '->' \'^'
Figure 7. Color variation ofHalgerda Okinawa. A. Photographed by Hachijo. B. Photographed by S. Kato. 2001.
C.PhotographedbyCarina Scheurs. D. PhotographedbyCarlsonandHoff. E.PhotographedbyR. Bolland.
tographedelsewhere show variation in theexternalcolorpattern (Fig. 7C-D). Differencesbetween
Halgerda Okinawa and H. graphica were discussed thoroughly by Carlson and Hoff(2000).
402 PROCEEDINGS OFTHE CALIFORNIAACADEMY OF SCIENCES
Volume 54, No. 23
Figures.RadularmoipholoLi\ ol// ,ikiiiu\ui (t ASI/ 144093).A.Sectionoftheradula.Scale=200|im.B.Outerlat-
eralteeth. Scale= 10\im. C. Innerlateral teeth. Scale=20^m. D. Middlelateral teeth. Scale=30|am.
Halgerda willeyi Eliot, 1904
(Figs 9-11)
=Halgerda willeyiin Coleman. 2001, p. 58, centerphoto,AMPI 117; andin Coleman, 1975 p. 63, Plate 170.
—
Material examined. CASIZ 144095, two specimens: 35 mm, 51 mm (dissected). 20 m
depth, collected by R. Nakano, March 2000; CASIZ 144096. three specimens; 25mm, 28 mm, 31
mm (dissected). 21 m depth, collected by R. Nakano, April 2000; CASIZ 144121, one specimen,
40 mm, dissected. 41.5 m depth. 1.3 km ENE Maeki-zaki, Seragaki, Okinawa, Ryukyu Islands,
Japan, collected by R. Holland, January 2001; CASIZ 144123, one specimen, 30 mm. 41.5 m
depth. 1.3 km ENE Maeki-zaki, Seragaki, Okinawa, Ryukyu Islands, Japan, collected by R.
Bolland, 8 December 2000; CASIZ 134919, one specimen, 74 mm. 43 m depth. 1.3 km ENE
Maeki-zaki, Seragaki, Okinawa, Ryukyu Islands, Japan, collected by R. Bolland, 17August 2000;
BMNH, one specimen, 60 mm. Intertidal. Bapper Bay, Aden, Yemen, leg. Sgt. Howse, RAMC.
October 1966.
—
Externalmorphology. Both specimens examined forthis study are externally similarto
other specimens ofH. willeyi published elsewhere. However, this species displays great variation
in external coloration (Figs. lOA-D; also see Goslineret al. 1996; Marshall andWillan 1999; Ono
1999; Coleman 1975, 2001; Bo—lland 2003; Rudman 2003).
Radular morphology. There were no differences noted in the radular morphology